Inhibition of mitogen-activated protein kinase and phosphatidylinositol 3-kinase activity in MCF-7 cells prevents estrogen-induced mitogenesis

Cell Growth and Differentiation

Volumn 11, Issue 2, 2000, Pages 99-110

  Lobenhofer, Edward K ^a   Huper, Gudrun ^a   Iglehart, J Dirk ^a   Marks, Jeffrey R ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; CYCLIN D1; DNA; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE B; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG; WORTMANNIN;

ARTICLE; CELL STRAIN MCF 7; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVITY; ENZYME INHIBITION; HORMONE ACTION; HUMAN; HUMAN CELL; IMMEDIATE EARLY GENE; MITOGENESIS; ONCOGENE C FOS; ONCOGENE C MYC; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADENOCARCINOMA; ANDROSTADIENES; BREAST NEOPLASMS; BUTADIENES; CHROMONES; CULTURE MEDIA, SERUM-FREE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIN D1; DEPRESSION, CHEMICAL; DNA REPLICATION; ENZYME ACTIVATION; ENZYME INHIBITORS; ESTRADIOL; ESTROGEN RECEPTOR MODULATORS; ESTROGENS; FEMALE; FLAVONOIDS; HUMANS; ISOQUINOLINES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; MITOSIS; MORPHOLINES; NEOPLASM PROTEINS; NEOPLASMS, HORMONE-DEPENDENT; NITRILES; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RETINOBLASTOMA PROTEIN; SULFONAMIDES;

MINK CELL FOCUS-FORMING VIRUS;

EID: 0034014355     PISSN: 10449523     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. Musgrove, E. A., and Sutherland, R. L. Cell cycle control by steroid hormones. Semin. Career Biol., 5: 381-389, 1994.
2. Musgrove, E., Wakeling, A., and Sutherland, R. Points of action of estrogen antagonists and a calmodulin antagonist within the MCF-7 human breast cancer cell cycle. Cancer Res., 49: 2398-2404, 1989.
3. Dubik, D., and Shiu, R. P. C. Mechanism of estrogen activation of c-myc oncogene expression. Oncogene, 7: 1587-1594, 1992.
4. Weisz, A., and Rosales, R. Identification of an estrogen response element upstream of the human c-fos gene that binds the estrogen receptor and the AP-1 transcription factor. Nucleic Acids Res., 18: 5097-5106, 1990.
5. 1-S phase progression is accompanied by increased cyclin D1 expression and decreased cyclin-dependent kinase inhibitor association with cyclin E-Cdk2. J. Biol. Chem., 272: 10882-10894, 1997.
6. Matsushime, H., Quelle, D. E., Shurtleff, S. A., Shibuya, M., Sherr, C. J., and Kato, J. Y. D-type cyclin-dependent kinase activity in mammalian cells. Mol. Cell. Biol., 14: 2066-2076, 1994.
7. Meyerson, M., and Harlow, E. Identification of G1 kinase activity for cdk6, a novel cyclin D partner. Mol. Cell. Biol., 14: 2077-2086, 1994.
8. Connell-Crowley, L., Harper, J. W., and Goodrich, D. W. Cyclin D1/ Cdk4 regulates retinoblastoma protein-mediated cell cycle arrest by site-specific phosphorylation. Mol. Biol. Cell, 8: 287-301, 1997.
9. Polyak, K., Kato, J. Y., Solomon, M. J., Sherr, C. J., Massaguθ, J., Roberts, J. M., and Koff, A. p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-β and contact inhibition to cell cycle arrest. Genes Dev., 8: 9-22, 1994.
10. Reynisdottir, I., Polyak, K., Iavarone, A., and Massaguθ, J. Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-β. Genes Dev, 9: 1831-1845, 1995.
11. DiDomenico, M., Castoria, G., Bilancio, A., Migliaccio, A., and Auricchio, F. Estradiol activation of human colon carcinoma-derived Caco-2 cell growth. Cancer Res., 56: 4516-4521, 1996.
12. Endoh, H., Sasaki, H., Maruyama, K., Takeyama, K., Waga, I., Shimizu, T., Kato, S., and Kawashima, H. Rapid activation of MAP kinase by estrogen in the bone cell line. Biochem. Biophys. Res. Commun., 235: 99-102, 1997.
13. ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells. EMBO J., 15: 1292-1300, 1996.
14. Singh, M., Setalo, G., Jr., Guan, X., Warren, M., and Toran-Allerand, C. D. Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: convergence of estrogen and neurotrophin signaling pathways. J. Neurosci., 19: 1179-1188, 1999.
15. Watters, J., Campbell, J., Cunningham, M., Krebs, E., and Dorsa, D. Rapid membrane effects of steroids in neuroblastoma cells: effects of estrogen on mitogen activated protein kinase signalling cascade and c-fos immediate early gene transcription. Endocrinology, 138: 4030-4033, 1997.
16. Parikh, I., Rajendran, K. G., Su, J. L., Lopez, T., and Sar, M. Are estrogen receptors cytoplasmic or nuclear? Some immunocytochemical and biochemical studies. J. Steroid Biochem., 27: 185-192, 1987.
17. Karthikeyan, N., and Thampan, R. V. Plasma membrane is the primary site of localization of the nonactivated estrogen receptor in the goat uterus: hormone binding causes receptor internalization. Arch. Biochem. Biophys., 325: 47-57, 1996.
18. Nadal, A., Rovira, J. M., Laribi, O., Leon-quinto, T., Andreu, E., Ripoll, C., and Soria, B. Rapid insulinotropic effect of 17β-estradiol via a plasma membrane receptor. FASEB J., 12:1341-1348, 1998.
19. Razandi, M., Pedram, A., Greene, G. L., and Levin, E. R. Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERα and ERβ expressed in Chinese hamster ovary cells. Mol. Endocrinol., 13:307-319, 1999.
20. Lee, H. W., and Eghbali-Webb, M. Estrogen enhances proliferative capacity of cardiac fibroblasts by estrogen receptor- and mitogen-activated protein kinase-dependent pathways. J. Mol. Cell. Cardiol., 30: 1359-1368, 1998.
21. Castoria, G., Barone, M. V., Di Domenico, M., Bilancio, A., Ametrano, D., Migliaccio, A., and Auricchio, F. Non-transcriptional action of oestradiol and progestin triggers DNA synthesis. EMBO J., 18: 2500-2510, 1999.
22. Fujimoto, J., Hori, M., Ichigo, S., Morishita, S., and Tamaya, T. Estrogen induces expression of c-fos and c-jun via activation of protein kinase C in an endometrial cancer cell line and fibroblasts derived from human uterine endometrium. Gynecol. Endocrinol., 10: 109-118, 1996.
23. Etindi, R. N., Manni, A., and Martel, J. The effects of TGF-α and 17β-estradiol on polyphosphoinositide metabolism in MCF-7 breast cancer cells. Breast Cancer Res. Treat., 24: 61-70, 1992.
24. Chen, D., Pace, P. E., Coombes, R. C., and Ali, S. Phosphorylation of human estrogen receptor a by protein kinase A regulates dimerization. Mol. Cell. Biol., 19: 1002-1015, 1999.
25. Vaughn, J. P., Davis, P. L., Jarboe, M. D., Huper, G., Evans, A. C., Wiseman, R. W., Berchuck, A., Iglehart, J. D., Futreal, P. A., and Marks, J. R. BRCA1 expression is induced before DNA synthesis in both normal and tumor-derived breast cells. Cell Growth Differ., 7: 711-715, 1996.
26. Vlahos, C. J., Matter, W. F., Hui, K. Y., and Brown, R. F. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem., 269: 5241-5248, 1994.
27. Toullec, D., Pianetti, P., Coste, H., Bellevergue, P., Grand-Perret, T., Ajakane, M., Baudet, V., Boissin, P., Boursier, E., and Loriolle, F. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J. Biol. Chem., 266: 15771-15781, 1991.
28. Chijiwa, T., Mishima, A., Hagiwara, M., Sano, M., Hayashi, K., Inoue, T., Naito, K., Toshioka, T., and Hidaka, H. Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino)ethyl]-5-isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J. Biol. Chem., 265: 5267-5272, 1990.
29. Alessi, D. R., Cuenda, A., Cohen, P., Dudley, D. T., and Saltiel, A. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem., 270: 27489-27494, 1995.
30. Imai, Y., Leung, C. K., Friesen, H. G., and Shiu, R. P. Epidermal growth factor receptors and effect of epidermal growth factor on growth of human breast cancer cells in long-term tissue culture. Cancer Res., 42: 4394-4398, 1982.
31. Wosikowski, K., Kung, W., Hasmann, M., Loser, R., and Eppenberger, U. Inhibition of growth factor-activated proliferation by antiestrogens and effects on early gene expression of MCF-7 cells. Int. J. Cancer, 53: 290-297, 1993.
32. Improta-Brears, T., Whorton, A. R., Codazzi, F., York, J. D., Meyer, T., and McDonnell, D. P. Estrogen-induced activation of mitogen-activated protein kinase requires mobilization of intracellular calcium. Proc. Natl. Acad. Sci. USA, 96: 4686-4691, 1999.
33. Ahn, N. G., Seger, R., and Krebs, E. G. The mitogen-activated protein kinase activator. Curr. Opin. Cell Biol., 4: 992-999, 1992.
34. Muise-Helmericks, R. C., Grimes, H. L., Bellacosa, A., Malstrom, S. E., Tsichlis, P. N., and Rosen, N. Cyclin D expression is controlled post-transcriptionally via a phosphatidylinositol 3-kinase/Akt-dependent pathway. J. Biol. Chem., 273: 29864-29872, 1998.
35. Dufourny, B., Alblas, J., van Teeffelen, H. A., van Schaik, F. M., van der Burg, B., Steenbergh, P. H., and Sussenbach, J. S. Mitogenic signaling of insulin-like growth factor I in MCF-7 human breast cancer cells requires phosphatidylinositol 3-kinase and is independent of mitogen-activated protein kinase. J. Biol. Chem., 272: 31163-31171, 1997.
36. Parker, M. G., Arbuckle, N., Dauvois, S., Danielian. P., and White, R. Structure and function of the estrogen receptor. Ann. NY Acad. Sci., 684: 119-126, 1993.
37. Ree, A. H., Landmark, B. F., Eskild, W., Levy, F. O., Lahooti, H., Jahnsen, T., Aakvaag, A., and Hansson, V. Autologous down-regulation of messenger ribonucleic acid and protein levels for estrogen receptors in MCF-7 cells: an inverse correlation to progesterone receptor levels. Endocrinology, 124: 2577-2583, 1989.
38. Read, L. D., Greene, G. L., and Katzenellenbogen, B. S. Regulation of estrogen receptor messenger ribonucleic acid and protein levels in human breast cancer cell lines by sex steroid hormones, their antagonists, and growth factors. Mol. Endocrinol., 3: 295-304, 1989.
39. Cicatiello, L., Sica, V., Bresciani, F., and Weisz, A. Identification of a specific pattern of "immediate-early" gene activation induced by estrogen during mitogenic stimulation of rat uterine cells. Receptor, 3: 17-30, 1993.
40. Hyder, S. M., Chiappetta, C., Murthy, L., and Stancel, G. M. Selective inhibition of estrogen-regulated gene expression in vivo by the pure antiestrogen ICI 182, 780. Cancer Res., 57: 2547-2549, 1997.
41. Planas-Silva, M. D., and Weinberg, R. A. Estrogen-dependent cyclin E-cdk2 activation through p21 redistribution. Mol. Cell. Biol., 17: 4059-4069, 1997.
42. Prall, O. W., Rogan, E. M., Musgrove, E. A., Watts, C. K., and Sutherland, R. L. c-Myc or cyclin D1 mimics estrogen effects on cyclin E-Cdk2 activation and cell cycle reentry. Mol. Cell. Biol., 18: 4499-508, 1998.
43. Foster, J. S., and Wimalasena, J. Estrogen regulates activity of cyclin-dependent kinases and retinoblastoma protein phosphorylation in breast cancer cells. Mol. Endocrinol., 10: 488-498, 1996.
44. Watts, C. K., Brady, A., Sarcevic, B., deFazio, A., Musgrove, E. A., and Sutherland, R. L. Antiestrogen inhibition of cell cycle progression in breast cancer cells in associated with inhibition of cyclin-dependent kinase activity and decreased retinoblastoma protein phosphorylation. Mol. Endocrinol., 9: 1804-1813, 1995.
45. Prall, O. W., Rogan, E. M., and Sutherland, R. L. Estrogen regulation of cell cycle progression in breast cancer cells. J. Steroid Biochem. Mol. Biol., 65: 169-174, 1998.
46. Ruzycky, A. L. Effects of 17β-estradiol and progesterone on mitogen-activated protein kinase expression and activity in rat uterine smooth muscle. Eur. J. Pharmacol., 300: 247-254, 1996.
47. Endoh, H., Sasaki, H., Maruyama, K., Takeyama, K., Waga, I., Shimizu, T., Kato, S., and Kawashima, H. Rapid activation of MAP kinase by estrogen in the bone cell line. Biochem. Biophys. Res. Commun., 235: 99-102, 1997.
48. Bonapace, I., Addeo, R., Altucci, L., Cicatiello, L., Bifulco, M., Laezza, C., Salzano, S., Sica, V., Bresciani, F., and Weisz, A. 17β-Estradiol overcomes a G1 block induced by HMG-CoA reductase inhibitors and fosters cell cycle progression without inducing ERK-1 and -2 MAP kinases activation. Oncogene, 12: 753-763, 1996.
49. Cullen, K. J., Yee, D., Bates, S. E., Brunner, N., Clarke, R., Dickson, R. E., Huff, K. K., Paik, S., Rosen, N., Valverius, E., et al. Regulation of human breast cancer by secreted growth factors. Acta Oncol., 28: 835-839, 1989.
50. El Yazidi, I., Renaud, F., Laurent, M., Courtois, Y., and Boilly-Marer, Y. Production and oestrogen regulation of FGF1 in normal and cancer breast cells. Biochim. Biophys. Acta, 1403: 127-140, 1998.
51. Zhang, L., Kharbanda, S., Chen, D., Bullocks, J., Miller, D. L., Ding, I. Y., Hanfelt, J., McLeskey, S. W., and Kern, F. G. MCF-7 breast carcinoma cells overexpressing FGF-1 form vascularized, metastatic tumors in ovariectomized or tamoxifen-treated nude mice. Oncogene, 15: 2093-2108, 1997.
52. Kim-Schulze, S., Lowe, W. L., Jr., and Schnaper, H. W. Estrogen stimulates delayed mitogen-activated protein kinase activity in human endothelial cells via an autocrine loop that involves basic fibroblast growth factor. Circulation, 98: 413-421, 1998.
53. Pacilio, C., Germano, D., Addeo, R., Altucci, L., Petrizzi, V. B., Cancemi, M., Cicatiello, L., Salzano, S., Lallemand, F., Michalides, R. J., Bresciani, F., and Weisz, A. Constitutive overexpression of cyclin D1 does not prevent inhibition of hormone-responsive human breast cancer cell growth by antiestrogens. Cancer Res., 58: 871-876, 1998.
54. Planas-Silva, M. D., Donaher, J. L., and Weinberg, R. A. Functional activity of ectopically expressed estrogen receptor is not sufficient for estrogen-mediated cyclin D1 expression. Cancer Res., 59: 4788-4792, 1999.
55. Jiang, S. Y., and Jordan, V. C. Growth regulation of estrogen receptor-negative breast cancer cells transfected with complementary DNAs for estrogen receptor [see comments]. J. Natl. Cancer Inst., 84: 580-591, 1992.
56. Levenson, A. S., and Jordan, V. C. Transfection of human estrogen receptor (ER) cDNA into ER-negative mammalian cell lines. J. Steroid Biochem. Mol. Biol., 51: 229-239, 1994.
57. Zajchowski, D. A., Sager, R., and Webster, L. Estrogen inhibits the growth of estrogen receptor-negative, but not estrogen receptor-positive, human mammary epithelial cells expressing a recombinant estrogen receptor. Cancer Res., 53: 5004-5011, 1993.
58. Gaben, A. M., and Mester, J. BALB/C mouse 3T3 fibroblasts expressing human estrogen receptor: effect of estradiol on cell growth. Biochem. Biophys. Res. Commun., 176: 1473-1481, 1991.
59. Kushner, P. J., Hort, E., Shine, J., Baxter, J. D., and Greene, G. L. Construction of cell lines that express high levels of the human estrogen receptor and are killed by estrogens. Mol. Endocrinol., 4: 1465-1473, 1990.
60. Touitou, I., Mathieu, M., and Rochefort, H. Stable transfection of the estrogen receptor cDNA into Hela cells induces estrogen responsiveness of endogenous cathepsin D gene but not of cell growth. Biochem. Biophys. Res. Commun., 169: 109-115, 1990.
61. Watts, C. K., Parker, M. G., and King, R. J. Stable transfection of the oestrogen receptor gene into a human osteosarcoma cell line. J. Steroid Biochem., 34: 483-490, 1989.
62. Diehl, J. A., Zindy, F., and Sherr, C. J. Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev., 11: 957-972, 1997.
63. Diehl, J. A., Cheng, M., Roussel, M. F., and Sherr, C. J. Glycogen synthase kinase-3β regulates cyclin D1 proteolysis and subcellular localization. Genes Dev., 12: 3499-3511, 1998.
64. Coffer, P. J., Jin, J., and Woodgett, J. R. Protein kinase B (c-Akt): a multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem. J., 335: 1-13, 1998.
65. Lavoie, J. N., L'Allemain, G., Brunet, A., Muller, R., and Pouyssegur, J. Cyclin D1 expression is regulated positively by the p42/p44MAPK and negatively by the p38/HOGMAPK pathway. J. Biol. Chem., 271: 20608-20616, 1996.
66. Lin, T. A., Kong, X., Haystead, T. A., Pause, A., Belsham, G., Sonenberg, N., and Lawrence, J. C., Jr. PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science (Washington DC), 266: 653-656, 1994.
67. Berthois, Y., Katzenellenbogen, J. A., and Katzenellenbogen, B. S. Phenol red in tissue culture media is a weak estrogen: implications concerning the study of estrogen responsive cells in culture. Proc. Natl. Acad. Sci. USA, 83: 2496-2500, 1986.